Vegetation phenology in spring has substantially advanced under climate warming, consequently shifting the seasonality of ecosystem process and altering biosphere–atmosphere feedbacks. However, whether and to what extent photoperiod (i.e., daylength) affects the phenological advancement is unclear, leading to large uncertainties in projecting future phenological changes. Here we examined the photoperiod effect on spring phenology at a regional scale using in situ observation of six deciduous tree species from the Pan European Phenological Network during 1980–2016. We disentangled the photoperiod effect from the temperature effect (i.e., forcing and chilling) by utilizing the unique topography of the northern Alps of Europe (i.e., varying daylength but uniform temperature distribution across latitudes) and examining phenological changes across latitudes. We found prominent photoperiod‐induced shifts in spring leaf‐out across latitudes (up to 1.7 days per latitudinal degree). Photoperiod regulates spring phenology by delaying early leaf‐out and advancing late leaf‐out caused by temperature variations. Based on these findings, we proposed two phenological models that consider the photoperiod effect through different mechanisms and compared them with a chilling model. We found that photoperiod regulation would slow down the advance in spring leaf‐out under projected climate warming and thus mitigate the increasing frost risk in spring that deciduous forests will face in the future. Our findings identify photoperiod as a critical but understudied factor influencing spring phenology, suggesting that the responses of terrestrial ecosystem processes to climate warming are likely to be overestimated without adequately considering the photoperiod effect.
- Award ID(s):
- 1702697
- NSF-PAR ID:
- 10339239
- Editor(s):
- Nelson, Karen E
- Date Published:
- Journal Name:
- PNAS Nexus
- Volume:
- 1
- Issue:
- 2
- ISSN:
- 2752-6542
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Temperate deciduous forests by definition include a large proportion of woody species that shed their leaves each autumn and are completely leafless during winter months. Leaf senescence in deciduous trees is an active, complex process typically involving the physiological formation of an abscission layer causing the petiole to mechanically detach from the branch. However, several deciduous species retain all or some senesced leaves on branches through much of winter, a phenomenon called leaf marcescence. Marcescence has long fascinated botanists, including Pehr Kalm as early as 1749. Yet, surprisingly little research has been done to date. Here, we review and explore patterns and mechanisms of leaf marcescence in temperate forests, bringing together six nonmutually exclusive but separately proposed hypotheses: (1) Marcescence has no adaptive function but rather an evolutionary byproduct; (2) Marcescent leaves deter winter browsing herbivores; (3) Leaf retention through winter improves nutrient resorption during autumn senescence; (4) Prolonged leaf shedding into spring minimizes nutrient leaching and promotes decomposition; (5) Marcescent leaves protect overwintering buds from frost or desiccation; and (6) Marcescent canopies provide winter cover for animals (including insects, birds, bats), thereby affecting plant nutrient availability via excrement. No hypothesis has complete support and few tests of multiple hypotheses have been done. It is likely that any adaptive value of marcescence is species and context dependent. Despite increased interest in plant phenology and prevalence of this trait, much remains to be understood on the physiology, evolution, function, and ecological implications of leaf marcescence.
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Summary In seasonally cold climates, many woody plants tolerate chilling and freezing temperatures by ceasing growth, shedding leaves and entering dormancy. At the same time, transport within these plants often decreases as the vascular system exhibits reduced functionality. As spring growth requires water and nutrients, we ask the question: how much does bud, leaf and flower development depend on the vasculature in spring? In this review, we present what is known about leaf, flower and vascular phenology to sort out this question. In early stages of bud development, buds rely on internal resources and do not appear to require vascular support. The situation changes during organ expansion, after leaves and flowers reconnect to the stem vascular system. However, there are major gaps in our understanding of the timing of vascular development, especially regarding the phloem, as well as the synchronization among leaves, flowers, stem and root vasculature. We believe these gaps are mainly the outcome of research completed in silo and urge future work to take a more integrative approach. We highlight current challenges and propose future directions to make rapid progress on this important topic in upcoming years.
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Methods Flower, leaf, and vascular phenology were monitored in pairs of precocious and non‐precocious congeners. Differences in resource allocation were quantified by measuring bud dry mass and water content throughout the year, floral hydration was modelled, and a girdling treatment completed on branches in the field.
Key Results Precocious flowering species invested more in floral buds the year before flowering than did their non‐precocious congeners, thus mobilizing less water in the spring, which allowed flowering before new vessel maturation.
Conclusions A shift in the timing of resource allocation in precocious flowering plants allowed them to flower before the production of mature vessels and minimized the significance of seasonal changes in vascular function to their flowering phenology. The low investment required to complete floral development in the spring when the plant vascular system is often compromised could explain why flowers can emerge before leaf out.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/pnasnexus/pgac046
